Energy transfer in the peridinin chlorophyll-a protein of Amphidinium carterae studied by polarized transient absorption and target analysis

Biophysical Journal

Volumn 80, Issue 6, 2001, Pages 2843-2855

  Krueger, Brent P ^a,c   Lampoura, Stefania S ^a   Van Stokkum, Ivo H M ^a   Papagiannakis, Emmanouil ^a   Salverda, Jante M ^a   Gradinaru, Claudiu C ^a   Rutkauskas, Danielis ^a   Hiller, Roger G ^b   Van Grondelle, Rienk ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b MACQUARIE UNIVERSITY   (Australia)

^c HOPE COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAROTENOID; CHLOROPHYLL A; PERIDININ; PIGMENT; UNCLASSIFIED DRUG;

ABSORPTION SPECTROPHOTOMETRY; AMPHIDINIUM CARTERAE; ANALYTIC METHOD; ANISOTROPY; ARTICLE; DINOFLAGELLATE; ENERGY TRANSFER; NONHUMAN;

AMPHIDINIUM CARTERAE; BACTERIA (MICROORGANISMS); DINOPHYCEAE; PROTEOBACTERIA; VIRIDIPLANTAE;

EID: 0035006465     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(01)76251-0     Document Type: Article

References (63)

1. Agarwal, R., B. P. Krueger, G. D. Scholes, M. Yang, J. Yom, L. Mets, and G. R. Fleming. 2000. Ultrafast energy transfer in LHC-II revealed by three-pulse photon echo peak shift measurements. J. Phys. Chem. B. 104:2908-2918.
2. Akimoto, S., S. Takaichi, T. Ogata, Y. Nishimura, I. Yamazaki, and M. Mimuro. 1996. Excitation energy transfer in carotenoid-cholorophyll protein complexes probed by femtosecond fluorescence decays. Chem. Phys. Lett. 260:147-152.
3. Andersson, P. O., S. M. Bachilo, R.-L. Chen, and T. Gillbro. 209. 1995. Solvent and temperature effects on dual fluorescence in a series of Carotenes: energy gap dependence of the internal conversion Rate. J. Phys. Chem. 99:16199-16116.
4. Andersson, P. O., R. J. Cogdell, and T. Gillbro. 1996. Femtosecond dynamics of carotenoid-to-bacteriochlorophyll a energy transfer in the light-harvesting antenna complexes from the purple bacterium Chromatium purpuratum. Chem. Phys. 210:195-217.
5. Andersson, P. O., and T. Gillbro. 1995. Photophysics and dynamics of the lowest excited singlet state in long substituted polyenes with implications to the very long-chain limit. J. Chem. Phys. 103:2509-2519.
6. Andersson, P. O., T. Gillbro, L. Ferguson, and R. J. Cogdell. 1991. Absorption spectral shifts of carotenoids related to medium polarizability. Photochem. Photobiol. 54:353-360.
7. Azumi, T., and S. P. McGlynn. 1965. Energy of excimer luminescence. III. Group theoretical considerations of molecular exciton and charge resonance states. J. Chem. Phys. 42:1675-1680.
8. Bautista, J. A., R. E. Connors, B. B. Raju, R. G. Hiller, F. P. Sharples, D. Gosztola, M. R. Wasielewski, and H. A. Frank. 1999a. Excited state properties of peridinin: observation of a solvent dependence of the lowest excited singlet state lifetime and spectral behavior unique among carotenoids. J. Phys. Chem. B. 103:8751-8758.
9. Bautista, J. A., R. G. Hiller, F. P. Sharples, D. Gosztola, M. R. Wasielewski, and H. A. Frank. 1999b. Singlet and triplet energy transfer in the peridinin-chlorophyll-a-protein from Amphidinium carterae. J. Phys. Chem. A. 103:2267-2273.
10. Brand, L., J. R. Knutson, L. Davenport, J. M. Beechem, R. E. Dale, D. G. Walbridge, and A. A. Kowalczyk. 1985. Time-resolved fluorescence spectroscopy: some applications of associative behavior to studies of proteins and membranes. In Spectroscopy and the Dynamics of Molecular Biological Systems. P. Bayley, and R. E. Dale, editors. Academic Press, London. 259-305.
11. Britton, G., and A. Young. 1993. Carotenoids in Photosynthesis. Chapman and Hall, London, New York. 498.
12. Carbonera, D., G. Giacometti, U. Segre, E. Hofmann, and R. G. Hiller. 1999. Structure-based calculations of the optical spectra of the light-harvesting peridinin - chlorophyll a - protein complexes from amphidinium carterae and heterocapsa pymaea. J. Phys. Chem. B. 103: 6349-6356.
13. Choi, S.-I., J. Jortner, S. A. Rice, and R. Silbey. 1964. Charge-transfer exciton states in aromatic molecular crystals. J. Chem. Phys. 41: 3294-3306.
14. 1 energies and dynamics of carotenoids. Chem. Phys. 194: 237-244.
15. Clayton, R. K. 1980. Photosynthesis: physical mechanisms and chemical patterns. Cambridge University Press, New York.
16. Damjanović A., T. Ritz, and K. Schulten. 1999. Energy transfer between carotenoids and bacteriochlorophylls in light-harvesting complex II of purple bacteria. Phys. Rev. E. 59:3293-3311.
17. Damjanović A., T. Ritz, and K. Schulten. 2000. Excitation energy transfer in the peridinin-chlorophyll-protein of Amphidinium carterae. Biophys. J. 79:1695-1705.
18. DeCoster, B., R. L. Christensen, R. Gebhard, J. Lugtenburg, R. Farhoosh, and H. A. Frank. 1992. Low-lying electronic states of carotenoids. Biochim. Biophys. Acta. 1102:107-114.
19. Dexter, D. L. 1953. A theory of sensitized luminescence in solids. J. Chem. Phys. 21:834-850.
20. Förster, T. 1948. Intermolecular energy transference and fluorescence. Ann. Phys. 2:55-75.
21. Förster, T. 1965. Delocalized excitation and excitation transfer. In Modern Quantum Chemistry. O. Sinanoglu, editor. Academic Press, New York. 93-137.
22. Frank, H. A., J. A. Bautista, J. Josue, Z. Pendon, R. G. Hiller, F. P. Sharples, D. Gosztola, and M. R. Wasielewski. 2000. Effect of the solvent environment on the spectroscopic properties and dynamics of the lowest excited states of carotenoids. J. Phys. Chem. B. 104:4569-4577.
23. Frank, H. A., and R. J. Cogdell. 1996. Carotenoids in photosynthesis. Photochem. Photobiol. 63:257-264.
24. Frank, H. A., R. Farhoosh, M. L. Aldema, B. Decoster, R. L. Christensen, R. Gebhard, and J. Lugtenberg. 1993. Carotenoid-to-bacteriochlorophyll singlet energy transfer in carotenoid-incorporated B850 light-harvesting complexes of Rhodobacter sphaeroides R-26.1. Photochem. Photobiol. 57:49-55.
25. Fujii, R., K. Onaka, M. Kuki, Y. Koyama, and Y. Watanabe. 1998. The 2A(g)(-) energies of all-trans-neurosporene and spheroidene as determined by fluorescence spectroscopy. Chem. Phys. Lett. 288:847-853.
26. Govindjee. 2000. Milestones in photosynthesis research. In Probing Photosynthesis: Mechanism, Regulation and Adaptation. M. Younis, U. Pathre, and P. Mohanty, editors. Taylor and Francis, London. 9-39.
27. Gradinaru, C. C., I. H. M. van Stokkum, A. A. Pascal, R. van Grondelle, and H. van Amerongen. 2000. Identifying the pathways of energy transfer between carotenoids and chlorophylls in LHCII and CP29: a multicolor, femtosecond pump-probe study. J. Phys. Chem. B. 104: 9330-9342.
28. Gradinaru, C. C., I. H. M. van Stokkum, R. van Grondelle, and H. van Amerongen. 1998. Ultrafast absorption changes of the LHCII carotenoids upon selective excitation of the chlorophylls. In Photosynthesis: Mechanisms and Effects. G. Garab, editor. Kluwer Academic Publishers, Dordrecht, The Netherlands. 277-280.
29. Harcourt, R. D., G. D. Scholes, and K. P. Ghiggino. 1994. Rate expressions for excitation transfer. II. Electronic considerations of direct and through-configuration exciton resonance interactions. J. Chem. Phys. 101:10521-10525.
30. Herek, J. L., T. Polivka, T. Pullerits, G. J. S. Fowler, C. N. Hunter, and V. Sundström. 1998. Ultrafast carotenoid band shifts probe structure and dynamics in photosynthetic antenna complexes. Biochemistry. 37: 7057-7061.
31. Hofmann, E., P. M. Wrench, F. P. Sharples, R. G. Hiller, W. Welte, and K. Diederichs. 1996. Structural basis of light harvesting by carotenoids: peridinin-chlorophyll-protein from Amphidinium carterae. Science. 272: 1788-1791.
32. Hudson, B. S., B. E. Kohler, and K. Schulten. 1982. Linear polyene electronic structure and potential surfaces. In Excited States. E. C. Lim, editor. Academic Press, New York. 1-95.
33. Jonas, D., M. J. Lang, T. Joo, Y. Nagasawa, Y. Jia, J. R. Norris, and G. R. Fleming. 1996. Pump-probe polarization anisotropy study of femtosecond energy transfer within the photosynthetic reaction center of Rhodobacter sphaeroides R26. J. Phys. Chem. 100:12660-12673.
34. Kleima, F. J., E. Hofmann, B. Gobets, I. H. M. van Stokkum, R. van Grondelle, K. Diederichs, and H. van Amerongen. 2000a. Forster excitation energy transfer in peridinin-chlorophyll-a-protein. Biophys. J. 78:344-353.
35. Kleima, F. J., M. Wendling, E. Hofmann, E. J. G. Peterman, R. van Grondelle, and H. van Amerongen. 195. 2000b. Peridinin chlorophyll a protein: relating structure and steady-state spectroscopy. Biochemistry. 39:5184-5185.
36. Koepke, J., X. Hu, C. Muenke, K. Schulten, and H. Michel. 1996. The crystal structure of the light-harvesting complex II (B800-850) from Rhodospirillum molischianum. Structure. 4:581-597.
37. Koutecky, J., and J. Paldus. 1963. A study of the interaction between two ethylene molecules by semi-empirical complete configuration interaction method in the π-electron approximation. Theor. Chim. Acta. 1:268-281.
38. Koyama, Y., M. Kuki, P. O. Andersson, and T. Gillbro. 1996. Singlet excited states and the light-harvesting function of carotenoids in bacterial photosynthesis. Photochem. Photobiol. 63:243-256.
39. Krueger, B. P., G. D. Scholes, I. R. Gould, and G. R. Fleming. 1999a. Carotenoid mediated B800-B850 coupling in LH2. Phys. Chem. Commun. 8:(http://www.rsc.org/ej/qu/1999/C9903172/index.htm)
40. Krueger, B. P., G. D. Scholes, R. Jimenez, and G. R. Fleming. 1998. Electronic excitation transfer from carotenoid to bacteriochlorophyll in the purple bacterium Rhodopseudomonas acidophila. J. Phys. Chem. B. 102:2284-2292.
41. 1 state of spheroidene in LH2 by two-photon fluorescence excitation. Chem. Phys. Lett. 310:57-64.
42. Kühlbrandt, W., D. N. Wang, and Y. Fujiyoshi. 1994. Atomic model of plant light-harvesting complex by electron crystallography. Nature. 367: 614-621.
43. McDermott, G., S. M. Prince, A. A. Freer, A. M. Hawthornthwaite-Lawless, M. Z. Papiz, R. J. Cogdell, and N. W. Isaacs. 1995. Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature. 374:517-521.
44. Mimuro, M., U. Nagashima, S. Takaichi, Y. Nishimura, I. Yamazaki, and T. Katoh. 1992. Molecular structure and optical properties of carotenoids for the in vivo energy transfer function in the algal photosynthetic pigment system. Biochim. Biophys. Acta. 1098:271-274.
45. 1 state of bacteriochlorophyll. J. Chem. Phys. 98:8012-8023.
46. Peterman, E. J. G., R. Monshouwer, I. H. M. van Stokkum, R. van Grondelle, and H. van Amerongen. 1997a. Ultrafast singlet excitation transfer from carotenoids to chlorophylls via different pathways in light-harvesting complex II of higher plants. Chem. Phys. Lett. 264: 279-284.
47. Peterman, E. J. G., T. Pullerits, R. van Grondelle, and H. van Amerongen. 1997b. Electron-phonon coupling and vibronic fine structure of light-harvesting complex II of green Plants: temperature dependent Absorption and high-resolution fluorescence spectroscopy. J. Phys. Chem. B. 101:4448-4457.
48. Polivka, T., J. L. Herek, D. Zigmantas, H.-E. Akerlund, and V. Sundström. 1999. Direct observation of the (forbidden) S1 state of carotenoids. Proc. Natl. Acad. Sci. U.S.A. 96:4914-4917.
49. Ricci, M., S. E. Bradforth, R. Jimenez, and G. R. Fleming. 1996. Internal conversion and energy transfer dynamics of spheroidene in solution and in the LH-1 and LH-2 light-harvesting complexes. Chem. Phys. Lett. 259:381-390.
50. - state energy on the conjugation length. J. Phys. Chem. B. 104:5011-5019.
51. Sashima, T., H. Nagae, M. Kuki, and Y. Koyama. 1999. A new singlet-excited state of all-trans-spheroidene as detected by resonance-Raman excitation profiles. Chem. Phys. Lett. 299:187-194.
52. - energy of crystalline all-trans-spheroidene as determined by resonance-Raman excitation profiles. Chem. Phys. Lett. 290:36-42.
53. Scholes, G. D., and G. R. Fleming. 2000. On the mechanism of light harvesting in photosynthetic purple bacteria: B800 to B850 energy transfer. J. Phys. Chem. B. 104:1854-1868.
54. Scholes, G. D., R. D. Harcourt, and G. R. Fleming. 1997. Electronic interactions in photosynthetic light-harvesting complexes: the role of carotenoids. J. Phys. Chem. B. 101:7302-7312.
55. Scholes, G. D., R. D. Harcourt, and K. P. Ghiggino. 1995. Rate expressions for excitation transfer. III. An ab initio study of electronic factors in excitation transfer and exciton resonance interactions. J. Chem. Phys. 102:9574-9581.
56. Schubert, W.-D., O. Klukas, N. Krauss, W. Saenger, P. Fromme, and H. T. Witt. 1997. Photosystem I of Synechococcus elongatus at 4 Å resolution: comprehensive structure analysis. J. Mol. Biol. 272:741-769.
57. Sharples, F. P., P. M. Wrench, K. Ou, and R. G. Hiller. 1996. Two distinct forms of the peridinin-chlorophyll a-protein from Amphidinium carterae. Biochim. Biophys. Acta. 1276:117-123.
58. Shreve, A. P., J. K. Trautman, H. A. Frank, T. G. Owens, and A. C. Albrecht. 1991. Femtosecond energy-transfer processes in the B800-B850 light-harvesting complex of Rhodobacter sphaeroides 2.4.1 Biochim. Biophys. Acta. 1058:280-288.
59. Sundström, V., T. Pullerits, and R. van Grondelle. 1999. Photosynthetic light-harvesting: reconciling dynamics and structure of purple bacterial LH2 reveals function of photosynthetic unit. J. Phys. Chem. B. 103: 2327-2346.
60. van Grondelle, R., J. P. Dekker, T. Gillbro, and V. Sundström. 1994. Energy transfer and trapping in photosynthesis. Biochim. Biophys. Acta. 1187:1-65.
61. van Stokkum, I. H. M., T. Scherer, A. M. Brouwer, and J. W. Verhoeven. 1994. Conformational dynamics of flexibility and semirigidly bridged electron donor-acceptor systems as revealed by spectrotemporal parameterization of fluorescence. J. Phys. Chem. 98:852-866.
62. Zechmeister, L. 1962. Cis-Trans Isomeric Carotenoids Vitamins A and Arylpolyenes. Springer-Verlag, Vienna.
63. Zhang, J.-P., R. Fujii, P. Qian, T. Inaba, T. Mizoguchi, Y. Koyama, K. Onaka, Y. Watanabe, and H. Nagae. 2000. Mechanism of the carotenoid-to-bacteriochlorophyll energy transfer via the Si state in the LH2 complexes from purple bacteria. J. Phys. Chem. B. 104:3683-3691.